Melanism evolution in the cat family is influenced by intraspecific communication under low visibility


Autoři: Maurício Eduardo Graipel aff001;  Juliano André Bogoni aff002;  Eduardo Luís Hettwer Giehl aff003;  Felipe O. Cerezer aff004;  Nilton Carlos Cáceres aff005;  Eduardo Eizirik aff006
Působiště autorů: Departamento de Ecologia e Zoologia, Centro de Ciências Biológicas, Universidade Federal de Santa Catarina, Florianópolis, Santa Catarina, Brazil aff001;  Laboratório de Ecologia, Manejo e Conservação de Fauna Silvestre (LEMaC), Escola Superior de Agricultura “Luiz de Queiroz”, Universidade de São Paulo, Piracicaba, São Paulo, Brazil aff002;  Programa de Pós-Graduação em Ecologia, Centro de Ciências Biológicas, Universidade Federal de Santa Catarina, Florianópolis, Santa Catarina, Brazil aff003;  Programa de Pós-Graduação em Biodiversidade Animal, CCNE, Universidade Federal de Santa Maria, Santa Maria, Rio Grande do Sul, Brazil aff004;  Departamento de Ecologia e Evolução, CCNE, Universidade Federal de Santa Maria, Santa Maria, Rio Grande do Sul, Brazil aff005;  Escola de Ciências da Saúde e da Vida, Pontifícia Universidade Católica do Rio Grande do Sul, Porto Alegre, Rio Grande do Sul, Brazil aff006
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0226136

Souhrn

Melanism in the cat family has been associated with functions including camouflage, thermoregulation and parasite resistance. Here we investigate a new hypothesis proposing that the evolution of melanism in cats has additionally been influenced by communication functions of body markings. To evaluate this hypothesis, we assembled a species-level data set of morphological (body marks: white marks on the backs of ears) and ecological (circadian activity: arrhythmic/nocturnal, and environmental preference: open/closed) characteristics that could be associated with communication via body markings, and combined these data with a dated molecular phylogeny. Next, we tested the association between melanism and communication, first by relating species’ body marks with their ecological conditions, using a Bayesian implementation of the threshold model. Second, to explore the evolution of characteristics potentially influencing melanism in cat species, we modeled their evolution relative to melanism using models of coordinated vs. independent character changes. Our results suggest that white marks are associated with intraspecific communication between individuals that have non-melanistic phenotypes, as well as towards melanistic individuals (without white marks). The absence of white marks in a melanistic individual tends to be a limiting condition for intraspecific visual communication at night, resulting in an evolutionary dilemma for these species, i.e. to be almost invisible at night, but not to communicate visually. The comparative analysis of several evolutionary models indicated more support for the evolution of melanism being coordinated with the evolution of arrhythmic activity and white marks on the backs of ears.

Klíčová slova:

Animal communication – Cats – Ears – Habits – Chronobiology – Leopards – Parasite evolution – Melanism


Zdroje

1. Majerus MEN. Melanism: evolution in action. Oxford: Oxford University Press. 1998.

2. Majerus MEN, Mundy NI. Mammalian melanism: natural selection in black and white. Trends Genet. 2003; 19: 585–588. doi: 10.1016/j.tig.2003.09.003 14585605

3. Schneider A, Henegar C, Day K, Absher D, Napolitano C, Silveira L, et al. Recurrent evolution of melanism in South American felids. PLoS genetics. 2015; 11(2): e1004892 doi: 10.1371/journal.pgen.1004892 25695801

4. Silva LG, Kawanishi K, Henschel P, Kittle A, Sanei A, Reebin A, et al. Mapping black panthers: Macroecological modeling of melanism in leopards (Panthera pardus). PloS One. 2017; 12(4): e0170378. doi: 10.1371/journal.pone.0170378 28379961

5. Werdelin L, Olsson L. How the leopard got its spots: a phylogenetic view of the evolution of felid coat patterns. Biol. J. Linn. Soc. 1997; 62: 383–400.

6. Allen WL, Cuthill IC, Scott-Samuel NE, Baddeley R. Why the leopard got its spots: relating pattern development to ecology in felids. Proc R Soc Biol Sci. 2011; 278: 1373–1380.

7. Rosenblum E, Hoekstra H, Nachman M. Adaptive reptile colour variation and the evolution of the MC1R gene. Evolution. 2004; 58: 1794–1808. https://doi.org/10.1111/j.0014-3820.2004.tb00462.x 15446431

8. Nachman MW, Hoekstra HE, D’Agostino SL. The genetic basis of adaptive melanism in pocket mice. Proc. Natl. Acad. Sci. USA. 2003; 100: 5268–5273. https://doi.org/10.1073/pnas.0431157100 12704245

9. McRobie HR, Moncrief ND, Mundy NI. Multiple origins of melanism in two species of North American tree squirrel (Sciurus). BMC Evolutionary Biology. 2019; 19(1): 140. doi: 10.1186/s12862-019-1471-7 31296164

10. Pardo-Diaz C, Salazar C, Baxter S, Merot C, Figueiredo-Ready W, Joron M, et al. Adaptive introgression across species boundaries in Heliconius butterflies. PLoS Genet. 2012; 8(6): e1002752. https://doi.org/10.1371/journal.pgen.1002752 22737081

11. Bittner T, King R, Kerfin J. Effects of body size and melanism on the thermal biology of garter snakes (Thamnophis sirtalis). Copeia. 2002; 2002: 59–68.

12. Tutt JW. Melanism and Melanochroism in British Lepidoptera, Swan Sonnenschein and Co. 1891.

13. Ortolani A, Caro TM. The adaptive significance of color patterns in carnivores: phylogenetic tests of classic hypotheses. In: Gittleman J. Editor. Carnivore behaviour, ecology and evolution, vol. 2, Ithaca, NY: Cornell University Press; 1996. pp. 132–188.

14. Caro T. The adaptive significance of coloration in mammals. BioScience. 2005; 55: 125–136.

15. Ortolani A. Spots, stripes, tail tips and dark eyes: predicting the function of carnivore colour patterns using the comparative method. Biol. J. Linn. Soc. 1999; 67: 433–476. https://doi.org/10.1111/j.1095-8312.1999.tb01942.x

16. Penteriani V, Delgado MM. The dusk chorus from an owl perspective: eagle owls vocalize when their white throat badge contrasts most. PLoS One. 2009; 4(4): e4960. doi: 10.1371/journal.pone.0004960 19352433

17. Penteriani V, Delgado MM, Campioni L, Lourenço R. Moonlight makes owls more chatty. PloS One. 2010; 5(1): e8696. doi: 10.1371/journal.pone.0008696 20098700

18. McComb K, Packer C, Pusey A. Roaring and numerical assessment in contests between groups of female lions, Panthera leo. Animal Behaviour. 1994; 47(2): 379–387.

19. Penteriani V, Delgado MM. Living in the dark does not mean a blind life: bird and mammal visual communication in dim light. Philosophical Transactions of the Royal Society B: Biological Sciences. 2017; 372(1717): 20160064.

20. Sillero-Zubiri C, MacDonald DW. Scent-marking and territorial behaviour of Ethiopian wolves Canis simensis. Journal of Zoology, London. 1998; 245: 351–361.

21. Gosling LM. A reassessment of the function of scent marking in territories. Zeitschrift für Tierpsychologie, Vienna. 1982; 2(60): 89–118.

22. Violle C. Navas ML, Vile D, Kazakou E, Fortunel C, Hummel I, et al. Let the concept of trait be functional! Oikos; 2007; 116(5): 882–892.

23. Graipel ME, Oliveira-Santos LGR, Goulart FVB, Tortato MA, Miller PRM, Cáceres NC. The role of melanism in oncillas on the temporal segregation of nocturnal activity. Braz J Biol. 2014; 74(3): S142–S145.

24. Galván I. Correlated Evolution of White Spots on Ears and Closed Habitat Preferences in Felids. Journal of Mammalian Evolution. 2019; 1–5.

25. Hortal J, Bello F, Diniz-Filho JAF, Lewinsohn TM, Lobo JM, Ladle RJ. Seven Shortfalls that Beset Large-Scale Knowledge of Biodiversity. Annual Review of Ecology, Evolution, and Systematics. 2015; 46(1): 523–549

26. Schneider A, David VA, Johnson WE, O’Brien SJ, Barsh GS, Menotti-Raymond M, et al. How the Leopard Hides Its Spots: ASIP Mutations and Melanism in Wild Cats. PloS One. 2012; 7(12): e50386. doi: 10.1371/journal.pone.0050386 23251368

27. Allen JA. Severtzow’s Classification of the Felidae. Bull. Am. Mus. Nat. Hist. 1919; 41: 335–340.

28. Bashir T, Bhattacharya T, Poudyal K, Sathyakumar S. Notable observations on the melanistic Asiatic Golden cat (Pardofelis temminckii) of Sikkim, India. NeBIO. 2011; 2(1): 2–4.

29. Werdelin L, Yamaguchi N, Johnson WE, O’Brien SJ. Phylogeny and evolution of cats (Felidae). In: Macdonald D, Loveridge A. (Eds). The Biology and Conservation of Wild Felids. Oxford University Press, Oxford, UK. 2010. pp. 59–82.

30. Felsenstein J. Using the quantitative genetic threshold model for inferences between and within species. Philosophical Transactions of the Royal Society B: Biological Sciences. 2005; 360(1459): 1427–1434.

31. Felsenstein J. A comparative method for both discrete and continuous characters using the threshold model. The American Naturalist. 2011; 179(2): 145–156. doi: 10.1086/663681 22218305

32. Revell LJ. Phytools: An R package for phylogenetic comparative biology (and other things). Methods Ecology and Evolution. 2012; 3: 217–223.

33. Revell LJ. Ancestral character estimation under the threshold model from quantitative genetics. Evolution. 2014; 68(3): 743–759. doi: 10.1111/evo.12300 24152239

34. Geweke J. Evaluating the accuracy of sampling‐based approaches to the calculation of posterior moments. In: Bernado JM, Berger JO, Dawid AP, Smith AFM. Editors. Bayesian Statistics 4. Clarendon Press, Oxford, UK. 1992.

35. Gelman A, Rubin DB. Inference from iterative simulation using multiples sequences. Statistical Science 1992; 7: 457–472.

36. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2016. https://www.R-project.org/.

37. Revell LJ. Phytools: an R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution. 2012; 3(2): 217–223.

38. Paradis E, Claude J, Strimmer K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics. 2004; 20(2): 289–290. doi: 10.1093/bioinformatics/btg412 14734327

39. Hackathon R, Bolker B, Butler M, Cowan P, De Vienne D, Eddelbuettel, D. Phylobase: Base package for phylogenetic structures and comparative data. R package version 0.6, 5. 2013.

40. Plummer M, Best N, Cowles K, Vines K. CODA: convergence diagnosis and output analysis for MCMC. R news. 2006; 6(1): 7–11.

41. Pagel M. Detecting correlated evolution on phylogenies: a general method for the comparative analysis of discrete characters. Proc. R. Soc. Biol. Sci.1994; 255(1342): 37–45.

42. Beaulieu JM, Donoghue MJ. 2013. Fruit evolution and diversification in campanulid angiosperms. Evolution. 2013 67(11): 3132–3144. doi: 10.1111/evo.12180 24151998

43. Li G, Davis BW, Eizirik E, Murphy WJ. Phylogenomic evidence for ancient hybridization in the genomes of living cats (Felidae). Genome Research. 2016; 26(1): 1–11. doi: 10.1101/gr.186668.114 26518481

44. Eizirik E, Yuhki N, Johnson WE, Menotti-Raymond M, Hannah SS, O’Brien SJ. Molecular genetics and evolution of melanism in the cat family. Current Biology. 2003; 13(5): 448–453. doi: 10.1016/s0960-9822(03)00128-3 12620197

45. Zanne AE, Tank DC, Cornwell WK, Eastman JM, Smith SA, FitzJohn RG, et al. Three keys to the radiation of angiosperms into freezing environments. Nature. 2014; 506(7486): 89–92 doi: 10.1038/nature12872 24362564

46. Silva LG, Oliveira TG, Kasper CB, Cherem JJ, Moraes EA, Paviolo A. Biogeography of polymorphic phenotypes: Mapping and ecological modelling of coat colour variants in an elusive Neotropical cat, the jaguarundi (Puma yagouaroundi). J. Zool. 2016; 299(4): 295–303.

47. Silva LG. Analise da distribuição espacial do melanismo na famılia Felidae em função de condicionantes ambientais. PhD Thesis, Pontifícia Universidade Católica do Rio Grande do Sul. 2014. http://repositorio.pucrs.br/dspace/handle/10923/5783

48. Anderson SR, Wiens JJ. Out of the dark: 350 million years of conservatism and evolution in diel activity patterns in vertebrates. Evolution. 2017; 71(8): 1944–1959. doi: 10.1111/evo.13284 28636789

49. Giordano AJ. 2016. Ecology and status of the jaguarundi Puma yagouaroundi: a synthesis of existing knowledge. Mammal Review. 2016; 46(1): 30–43.

50. Van Schaik CP, Griffiths M. Activity Periods of Indonesian Rain Forest Mammals Biotropica. 1996; 28: 105–112.

51. Azlan JM, Sharma DS. The diversity and activity patterns of wild felids in a secondary forest in Peninsular Malaysia. Oryx. 2006; 40(01): 36–41.

52. Kawanishi K, Sunquist ME, Eizirik E, Lynam AJ, Ngoprasert D, Wan Shahruddin WN, et al. Near fixation of melanism in leopards of the Malay Peninsula. J. Zool. 2010; 282: 201–206.

53. Hayward MW, Slotow R. Temporal partitioning of activity in large African carnivores: tests of multiple hypotheses. South Afr. J. Wildl. Res. 2009; 39(2): 109–125.

54. Gippoliti S, Meijaard E. Taxonomic uniqueness of the Javan Leopard; an opportunity for zoos to save it. Contrib Zool. 2007; 76: 55–58.

55. Oliveira-Santos LGR, Graipel ME, Tortato MA, Zucco CA, Cáceres NC, Goulart FV. Abundance changes and activity flexibility of the oncilla, Leopardus tigrinus (Carnivora: Felidae), appear to reflect avoidance of conflict. Zoologia. 2012; 29(2): 115–120.

56. Forsman A, Ahnesjö J, Caesar S, Karlsson M. A model of ecological and evolutionary consequences of color polymorphism. Ecology. 2008; 89(1): 34–40. doi: 10.1890/07-0572.1 18376544

57. Paviolo AN, Di Blanco YE, De Angelo CD, Di Bitetti MS. Protection affects the abundance and activity patterns of pumas in the Atlantic forest. Journal of Mammalogy. 2009; 90: 926–934.

58. Brodie JF. Is research effort allocated efficiently for conservation? Felidae as a global case study. Biodiversity and Conservation. 2009; 18(11): 2927–2939.


Článek vyšel v časopise

PLOS One


2019 Číslo 12